Directed ultrafast conformational changes accompany electron transfer in a photolyase as resolved by serial crystallography
Cellini, A., Shankar Madan, K., Nimmrich, A., Hunt Leigh, A., Monrroy, L., Mutisya, J., Furrer, A., Beale, E. V., Carrillo, M., Malla Tek, N., Maj, P., Vrhovac, L., Dworkowski, F., Cirelli, C., Johnson, P. J. M., Ozerov, D., Stojković, E. A., Hammarström, L., Bacellar, C., . . . Westenhoff, S. (2024). Directed ultrafast conformational changes accompany electron transfer in a photolyase as resolved by serial crystallography. Nature Chemistry, Early online. https://doi.org/10.1038/s41557-023-01413-9
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2024Copyright
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Charge-transfer reactions in proteins are important for life, such as in photolyases which repair DNA, but the role of structural dynamics remains unclear. Here, using femtosecond X-ray crystallography, we report the structural changes that take place while electrons transfer along a chain of four conserved tryptophans in the Drosophila melanogaster (6-4) photolyase. At femto- and picosecond delays, photoreduction of the flavin by the first tryptophan causes directed structural responses at a key asparagine, at a conserved salt bridge, and by rearrangements of nearby water molecules. We detect charge-induced structural changes close to the second tryptophan from 1 ps to 20 ps, identifying a nearby methionine as an active participant in the redox chain, and from 20 ps around the fourth tryptophan. The photolyase undergoes highly directed and carefully timed adaptations of its structure. This questions the validity of the linear solvent response approximation in Marcus theory and indicates that evolution has optimized fast protein fluctuations for optimal charge transfer.
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https://converis.jyu.fi/converis/portal/detail/Publication/202860539
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S.W. acknowledges the European Research Council for support (grant number 279944). We acknowledge the Paul Scherrer Institute, Villigen, Switzerland, for provision of free-electron laser beamtime at the Alvra instrument of the SwissFEL ARAMIS branch. M.S. acknowledges support by NSF-STC-1231306 (BioXFEL), J.A.I. by the Academy of Finland (grant number 332742), L.H. by the Knut and Alice Wallenberg Foundation (grant number 2019.0071), E.A.S. by the NSF-STC-123306 (BioXFEL) subaward 6227, T.W. by project grant 310030:197674 of the Swiss National Science Foundation and M.C. by the Swiss Nanoscience Institute (grant number 1904). M.K.S. acknowledges Herbert and Karin Jacobson Foundation and Längmanska Kulturfonden (BA23-0489) for funding. ...License
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